Revealing the diversity of Parasmittina Osburn, 1952 (Bryozoa, Cheilostomatida) from the Southwest Atlantic: Species complexes, non-native and new species

Parasmittina is the most representative cheilostome genus of the family Smittinidae, often reported in the fouling non-indigenous marine community. Here, we present a review of Parasmittina species reported in the Southwestern Atlantic including the characterization of one species from Argentina (P. dubitata) and ten from the Brazilian coast: P. abrolhosensis, P. alba, P. bimucronata, P. ligulata comb. nov., P. longirostrata, P. pinctatae, P. serrula, P. simpulata, P. winstonae and the new species Parasmittina falciformis sp. nov. The new species is characterized by a smooth distally primary orifice with 1–2 oral spines, large lyrula, serrated condyles with hooked tips, and two types of avicularia–small and subtriangular and large sublanceolate. This study does not recognize four species previous recorded in Brazil: reports of P. betamorphaea and P. trispinosa are now assigned to P. pinctatae; records of P. munita belong to P. falciformis sp. nov.; and reports of P. spathulata encompass at least two taxa, including P. abrolhosensis and P. simpulata. In this study, five species complexes (P. alba, P. longirostrata, P. serrula, P. simpulata and P. winstonae) were identified and require further investigations. While six species characterized here were first described based on specimens from the Southwestern Atlantic (P. abrolhosensis, P. alba, P. dubitata, P. ligulata comb. nov., P. simpulata and P. falciformis sp. nov.), the remaining species are mainly known from the Indo-Pacific. These taxa are here recognized as exotic (P. longirostrata) and cryptogenic (P. bimucronata, P. pinctatae, P. serrula and P. winstonae) in the studied area. Most of the non-native taxa are widespread along the Brazilian coast, growing on both artificial and natural surfaces, indicating that they are well-established in the area. As non-native bryozoans can negatively influence the environment, affecting human economic activities and beach usage, further studies on the fauna presented here are suggested to determine the origin of these taxa and help prevent bioinvasion events along the SW Atlantic.

Like most cheilostome bryozoans, smittinids have short-living, non-planktotrophic larvae with limited active dispersal over long distances (e.g., [14,15]).However, certain taxa, including Parasmittina species, have been reported far from their expected natural geographic distribution, indicating association with bioinvasion events (e.g., [4,9,16,17]).Therefore, the accurate taxonomic identification of these taxa represents the first step in detecting and tracking potential invasions (e.g., [14,15]).However, the taxonomy of several Smittinidae taxa may be puzzling, sometimes leading to generic misassignments, notably in the case of Parasmittina (e.g., [4,[18][19][20]).Studies on smittinids from Brazil, in the SW Atlantic, have resulted in morphological redefinitions of Hemismittoidea, Smittoidea, and Parasmittina [4].These redifinitions facilitate the differentiation between these genera, indicating that Parasmittina comprises smittinids with an imperforate frontal shield, none to many spines, and avicularia with variable morphology and sizes placed proximolateral or distolateral to the orifice [4].Similar to genus delimitation, species distinctions can be also problematic, particularly when only colonial fragments are available.These specimens may obscure variations related to colonial development in different ontogenetic stages, making it challenging to differentiate distinct morphospecies [4,9,21].
Eleven species of Parasmittina have been reported from the SW Atlantic: P. abrolhosensis Ramalho, Taylor (Hincks, 1884), P. simpulata Winston, Vieira & Woollacott, 2014, P. spathulata (Smitt, 1873) and P. trispinosa (Johnston, 1838) [22].Among these, P. munita, P. spathulata and P. trispinosa have been assigned to be part of the P. trispinosa complex [5,23,24].Although first described based on specimens from the Northeastern Atlantic, P. trispinosa has been historically reported in different oceans with different morphologies attributed to intraspecific variations (e.g., P. trispinosa var.loxa and P. trispinosa var.spathulata).However, Soule & Soule [5] reviewed historical records of P. trispinosa using scanning electron microscopy (SEM), assigning them to 14 species, eight of which were described as new species.The need for taxonomic reviews in some of these taxa was previously indicated by Vieira et al. [25], Almeida et al. [26] and Farias et al. [4].In this context, here we reexamined SW Atlantic specimens assigned to the genus Parasmittina, providing morphological characterization and assessing the exotic status of 12 species, including the description of a new species.Additionally, a tabular identification key with almost all species of the genus is provided.

Material and methods
All necessary permits for the new samples were obtained for the described field studies in Brazil (collecting permit number 47108 SISBIO/Instituto Chico Mendes de Conservac ¸ão da Biodiversidade).The new samples in reported localities do not include protected areas and did not involve endangered or protected species.Permissions from all museums were obtained to access and study their collections.
Type and non-type specimens studied here are deposited in the Bryozoa collections of the Setor de Zoologia do Museu de Histo ´ria Natural da Bahia, Universidade Federal da Bahia, Salvador, Brazil (UFBA); Departamento de Zoologia, Universidade Federal de Pernambuco, Recife, Brazil (UFPE); Museu de Zoologia, Universidade de São Paulo (MZUSP); Smithsonian Institution National Museum of Natural History, Washington D.C., USA (USNM); Natural History Museum, London, United Kingdom (NHMUK); and Museum fu ¨r Naturkunde, Berlin, Germany (MFN).The specimen from Argentina was analyzed based on scanning electron microscope (SEM) micrographs provided by Juan Lo ´pez Gappa.
Non-type specimens were first washed in sodium hypochlorite and then immersed in water for surface cleaning using a thin brush.These specimens were air-dried before examination under a stereoscopic microscope for the description of external morphology and delimitation of morphotypes.Selected specimens of each morphotype were mounted on stubs, coated with gold, and analyzed with a SEM JEOL JSM-6390LV at the Centro de Pesquisa Gonc ¸alo Moniz, FIOCRUZ, Bahia, Brazil.Some unbleached specimens deposited at the NHMUK and USNM were examined using a SEM equipped with a low-vacuum chamber and back-scattered electron detector, using a SEM LEO 1455-VP and PhilipsXL30, respectively.
The determination of the native/exotic status of the studied species was conducted following the criteria described by Chapman & Carlton [29,30] and adapted for Bryozoa by Miranda et al. [15] and Xavier et al. [31].

Nomenclatural acts
The electronic edition of this article conforms to the requirements of the amended International Code of Zoological Nomenclature, and hence the new names contained herein are available under that Code from the electronic edition of this article.This published work and the nomenclatural acts it contains have been registered in ZooBank, the online registration system for the ICZN.The ZooBank LSIDs (Life Science Identifiers) can be resolved, and the associated information viewed through any standard web browser by appending the LSID to the prefix "http://zoobank.org/".The LSID for this publication is: urn:lsid:zoobank.org:pub:FEC88DB2-877B-46E4-94C0-DEF4C8F449BD.The electronic edition of this work was published in a journal with an ISSN, and has been archived and is available from the following digital repositories: LOCKSS (added: Sep 10 2012 6:55PM UTC) [http://www.lockss.org];PubMed Central (added: Sep 10 2012 6:55PM UTC) [http://www.ncbi.nlm.nih.gov/pmc].

Genus Parasmittina Osburn, 1952
Type species.Lepralia jeffreysi Norman, 1876, by original designation.Diagnosis.Autozooids with imperforate frontal wall, except for marginal pores.Primary orifice with smooth or beaded distal margin, oral spines usually present, lyrula of variable size and condyles with distinct profiles.Secondary orifice with variable development, sometimes with a proximal pseudosinus.Adventitious avicularia formed from a marginal pore [for example, as in P. jeffreysi (acc.Winston & Hayward [33]), P. nitida and P. winstonae], or sometimes, from a latero-oral pore (for example, as in P. pinctatae, P. simpulata and P. falciformis sp.nov.); adventitious avicularia with diverse shapes and positions (frontal, latero-oral or marginal), but never suboral, unless if displaced by the secondary calcification.Vicarious avicularia may also be present.Ovicells hyperstomial, initially prominent and becoming immersed with secondary calcification; ectooecium with pseudopores (modified from Osburn [24]).
Thus, in this study, we attempt to analyze colonies at various astogenetic stages, comparing them with all congeners reported worldwide and using both morphological and morphometric data.Diagnostic features were based mainly on the primary orifice (distal margin ornamentation, number of spines, lyrula width, and condyles morphology), avicularia (if adventitious and/or interzooidal, placement, orientation, size, and morphologies), and ooecia (number of pseudopores, and secondary calcification).1E, 2B and 2E) present at one or both side of the orifice, unequal in size if paired, placed below to the secondary orifice, proximally oriented, rostrum narrow and slightly curved, smooth to slightly corrugated at its lateral margins, rounded tip, palate occupying about half of the rostrum length and oblong foramen; (2) small, subtriangular, bulbous avicularia (Fig 1A and 1D), placed laterally at one side of the orifice, proximally oriented, rostrum subtriangular, pointed tip, palate narrow, reaching twice its initial size with colonial development, leaving a sublanceolate profile; (3) small, narrow and subtriangular to elliptic avicularia (Figs 1C and 1E, 1F, 2B and 2E), placed in zooidal margins and/ or in the frontal wall, with smooth lateral margins, rounded tip, palate narrow and elliptical foramen; (4) large spatulate avicularia, more common in older zooids, placed proximolaterally below the orifice, oriented proximally, with rounded distal edge, palate broad, foramen subtriangular, elongate rostrum, with smooth margins and crossbar complete, with 3-  2F); ectooecium with 18-25 small pseudopores (0.003-0.005-0.008mm in diameter; n = 30; SD = 0.001 mm), mainly placed at the distal region of the ectooecium surface.

ZW
Parasmittina areolata was originally described by Canu & Bassler [41] based on specimens from Hawaii, Pacific Ocean.However, it has been reported in Brazilian coast and in the Caribbean [3,37,40].Here we analyzed the type of P. areolata (USNM 8443), Smittina areolata, holotype, F. Canu & R. Bassler det., Molokai, Hawaii, 142-406 m, coll.1902, Fig 3A -3D), revealing that this species is not conspecific with the Brazilian material.Parasmittina areolata has a double row of areolar pores (single in specimens from Brazil), low secondary orifice (with lateral flaps in Brazilian material) and ectooecium centrally perforated (distally perforated in specimens from Brazil).The morphologically related species P. spathulata is distinct from the Brazilian material in having a broader lyrula (acc.Winston [7]).Specimens from the Caribbean previously attributed to P. areolata by Winston [37] were reassigned to P. luteoserrula Winston & Jackson, 2021 (see Winston & Jackson [13]), distinct from Brazilian specimens by having an orifice with a serrated distal margin, and a large avicularium with a coarsely serrated margin.
Specimens studied here shares most of the diagnostic characters provided by Ramalho et al. [11] in the description of P. abrolhosensis, including a primary orifice with distal margin smooth, lyrula narrow and robust and down-curved hooked condyles with serrated margins; secondary orifice with a U-shaped pseudosinus; avicularia with four morphologies: (1) small, narrow and elongate, (2) small, subtriangular and bulbous [not described by Ramalho et al. [11], but figured in 3H], (3) small, narrow and subtriangular to elliptic, and (4) large spatulate; and ovicells densely surrounded by adjacent frontal wall in older colonies, and with small pseudopores.However, specimens from Ramalho et al. [11] have 3-4 oral spines (1-3 in colonies studied here) and the large avicularium was not found as vicarious.Interestingly, the original description of P. abrolhosensis was based on three small colonial fragments inhabiting corals (acc.Ramalho et al. [11], Figs 3H, 4A-4D) whereas several colonies studied here are from artificial substrata and material from Canu & Bassler [40] are colonies with rough secondary calcification.Since the number of oral spines and occurrence of avicularia in Parasmittina are very variable in relation to colony development and habitat (e.g., [2,4,5,9,21,39]), these differences are likely to be intraspecific variations of P. abrolhosensis rather than a different species.

Parasmittina alba
Remarks.Parasmittina alba was described based on specimens from Rio de Janeiro, SE Brazil; it was characterized by having a granular frontal wall, condyles with hooked tips, large lyrula, 1-2 oral spines, secondary orifice with lateral projections and pseudosinus, avicularia latero-oral (small subtriangular or rounded), large (spatulate) and interzooidal (subtriangular), with only one avicularium occurring per zooid, and ectooecium with pseudopores [10].Most of these morphological characters are also seen in colonies from SE and NE Brazil examined here, despite the presence of 1-3 orificial spines and the rare presence of interzooidal avicularia.Most of our examined material form small patches growing on ceramic experimental tile plates (specimens from northeastern Brazil; Fig 4A), but the larger specimens have been only observed growing on rhodoliths (specimens from southeastern Brazil; Fig 4F).The avicularia were often found in older part of the colonies (Fig 4F ) when comparing with the growing zone with the new zooids (Fig 4B ), suggesting the formation of the avicularia in later colony astogeny.Moreover, we found no morphometric differences in colonies studied here assigned and other records of P. alba (Table 2).
Parasmittina alba was reported as a non-indigenous species in Portugal, Northeastern Atlantic [17].Souto et al. [17] noted slight variations between specimens from Rio de Janeiro (acc.Ramalho et al. [10]) and those from Portugal, including smaller ectooecial pseudopores related with more significant calcification, the occurrence of two avicularia in ovicelled zooids and absence of interzooidal avicularia.Additionally, Souto et al. [17] suggested that P. alba could be assigned as a junior synonym of P. betamorphaea Winston, 2005 [7] described from the United States (Northwestern Atlantic) since characters used to distinguish these taxa are very variable among colonies and zooids (i.e., number of avicularia, calcification of margins and rostrum of the avicularia).The Caribbean P. lavela Soule & Soule [5] also shares most morphological diagnostic features of P. alba.These taxa have a granular frontal calcification, primary orifice without distal denticles, with large lyrula and thin down-curved hooked condyles, secondary orifice with a short pseudosinus, and ooecium with merged pseudopores [5].The only difference between P. alba and P. lavela is the presence of a single morphotype of avicularia in P. lavela (i.e., small subtriangular latero-oral avicularia), lacking all other types described to P. alba.Soule & Soule [9] stated that avicularia are not common in P. lavela, but only a tiny single specimen growing on algae on an anchor chain was examined [5], somewhat corroborating morphological variation and biological associations already reported [10,17] and assigned here to P. alba.Avicularia are known to be very variable in Smittinidae according to colony development and habitat (e.g., [2,4,5,9,21,39]).Avicularia morphology is quite variable in specimens of P. alba here examined.We suspect that P. alba and P. betamorphea may represent different astogenetic variations of P. lavela-specimens of P. alba comprising a stage with all types of avicularia, ovicells, and secondary calcification [10], whereas P. betamorphea could represent young colony that lacks ovicells and have few avicularia [7].
Zooidal measurements of specimens attributed to P. alba and P. betamorphea are like those of P. lavela (Table 2).In addition, a peculiar feature of the species (as already mentioned by Souto et al. [17]) is a notch on the distal margin of the primary orifice of ovicellate zooids-this notch is formed in the place where the oral spines were inserted (Fig 4E ) [see Ramalho et al. [10] (Fig 2G ) and Souto et al. [17] (Fig 3B )].However, observing this notch in colonies of P. lavela and P. betamorphea was impossible.Ovicelled zooids of P. lavela had the distal margin of the primary orifice occluded by secondary calcification [5] and P. betamorphea lacks ovicells [7].Thus, at least one species complex involving P. alba, P. betamorphea, and P. lavela can be recognized (Table 2).
Finally, another congener may be involved in this complex.Specimens from the Southeast and Northeast Atlantic, as well as from the Mediterranean attributed to Parasmittina protecta (Thornely, 1905) (acc.Harmelin et al. [9]) also share most morphological diagnostic features of P. alba, being only variable in avicularia morphotypes occurrence.However, P. protecta was first described with colonies from the Indian Ocean and the original description is brief, not including diagnostic features of the primary orifice (distal margin ornamentation, condyles, lyrula) and detailed characterization of avicularia (acc.Thornely [43]).Also, there is no redescription of type or topotype specimens, preventing us from reliably characterizing P. protecta from Thornely (1905).Additional studies including more specimens are required to identify whether P. protecta and P. alba belong to the same species.
Remarks.Parasmittina dubitata was first described based on specimens from Burdwood Bank, Argentina, growing on organic carbonates [49].Here, we provide characterization of a single specimen from Tierra del Fuego, Argentina, kindly sent by Juan Lopez Gappa (pers.comm.2021), that exhibts the diagnostic characters of the original description of P. dubitata.This species is readily distinguished from other congeners by the primary orifice morphology, including a lyrula with a concave distal margin and rounded condyles, unlike the straight lyrula and triangular to hooked condyles of most Parasmittina species.

Parasmittina ligulata (Ridley
Parasmittina ligulata comb.nov.was originally described based on specimens from southeastern Brazil, but later synonymized under P. spathulata by Vieira et al. [25], who also include in the same synonym list Brazilian specimen attributed to Smittina trispinosa spathulata (USNM 8558).As stated above, the specimen studied by Canu & Bassler [40] belongs to P. abrolhosensis.Also, the analysis of the syntype showed that P. ligulata comb.nov.can be readily differentiated from P. spathulata and P. abrolhosensis by showing large, avicularia elongate to sublanceolate avicularia (spatulate in the other species).Other differences between P. ligulata comb.nov.and P. spathulata is lyrula size (occupying one-quarter of the orifice in P. ligulata comb.nov.and half of the orifice in P. spathulata), and between P. ligulata comb.nov.and P. abrolhosensis is the occurrence of small latero-oral subtriangular avicularia in P. abrolhosensis (absent in P. ligulata comb.nov.).
Among all congeners, P. ligulata comb.nov.most resembles Parasmittina longirostrata Liu in Liu, Yin & Ma, 2001 [45] mainly because of small proximolateral, elongate and large sublanceolate avicularia.However, these species are distinguished by lyrula size (occupying about one-quarter of the orifice in P. ligulata comb.nov.and half of the orifice in P. longirostrata) and small oblong avicularia (absent in P. ligulata comb.nov.and very common in P. longirostrata).

Parasmitina longirostrata
Remarks.Parasmittina longirostrata is characterized by the combination of a primary orifice with smooth distal margin, with 3-4 oral spines, lyrula median-sized, secondary orifice forming a U-shaped pseudosinus, and two types of proximolateral avicularia: small, elongate and thin, and large, sub-lanceolate with crenulated margins [45].
Liu et al. [45] considered that P. serrula Soule & Soule, 1973 [2] was the most similar congener to P. longirostrata probably because of having two types of avicularia with the smaller and proximolateral being thin and narrow.However, several differences are observed between these species, including the primary orifice (with smooth distal margin and lyrula occupying half of the orificial width in P. longirostrata and with distal denticles and lyrula occupying onequarter of the orificial width in P. serrula), placement of the smaller avicularia (typically straightly placed proximolateral to the orifice in P. longirostrata and transversally below the orifice in P. serrula) and profile of the large avicularium (sublanceolate in P. longirostrata and lanceolate with lobate edge at half distal part in P. serrula).A congener very similar to P. longirostrata, however, is P. serruloides Harmelin et al. 2009 [9], described based on specimens from the Mediterranean.These species are only distinguished by the profile of the condyles (robust and with 4-7 teeth in P. longirostrata, but thin and with 2-5 teeth in P. serruloides).However, the profile of the condyles can be variable within a colony, as already seen in other Parasmittina (e.g., P. onychorrhyncha Ryland & Hayward, 1992 and P. aleutensis Soule & Soule, 2002).Thus, despite the type locality of P. longirostrata being in the North Pacific.The morphology and morphometry of the specimens from Brazil resemble those of specimens of P. longirostrata from China [45], but the autozooids of P. serruloides appear to be smaller zooids when compared with P. longirostrata (Table 4).However, further studies are needed with specimens from the Mediterranean, to determine if there are intraspecific differences that justify the synonymization of P. serruloides with P. longirostrata Distribution.Northeastern Pacific: China [45]; SW Atlantic: Brazil (present study).Specimens from Lebanon [9] need to be compared to ascertain the synonym with P. longisrostrata.[18].Non Smittia egyptiaca Waters, 1909: 157 [52].
Parasmittina pinctatae differs from P. trispinosa in the profile of the primary orifice (as long as wide in P. pinctatae and longer than wide in P. trispinosa), number of oral spines (1-2 in Parasmittina pinctatae and 2-3 in P. trispinosa), profile of avicularia (the proximolateral is subtriangular in P. pinctatae and oblong in P. trispinosa; the large is spatulate in P. pinctatae and subtriangular in P. trispinosa), and number of ovicell pseudopores (more than 20 in P. pinctatae and 2-4 in P. trispinosa) [5].Differences between P. pinctatae and P. nitida include the profile of the primary orifice (subcircular in P. pinctatae and rounded in P. nitida), lyrula (median in P. pinctatae and narrow in P. nitida), types of avicularia (three types in P. pinctatae: proximolateral, marginal and large; two types in P. nitida: proximolateral and marginal) and orientation of the proximolateral avicularia (distolateral in P. pinctatae and proximolateral in P. nitida) [55].Finally, P. pinctatae is distinguished from P. betamorphea in having a narrower lyrula (the lyrula of P. betamorphaea is twice the length of that from of P. pinctatae) and condyles thin and almost straight (robust and curved in P. betamorphaea) [7].
The taxonomic history of P. pinctatae needs to be explained.Liu et al. [45] attributed other specimens from China to P. parsevalii (Audouin, 1826) due to these having avicularia placed at the frontal wall and laterally to the orifice (not associated with the peristome like in P. pinctatae) and differences in ooecia surface.However, P. parsevalii sensu Liu et al. [45] differs from P. parsevalii (acc.Hayward & Parker [47]) by having a primary orifice with smooth distal margin (beaded in P. parsevalii), relatively wide and low lyrula (narrow and high in P. parsevalii), almost straight and thin condyles (robust and hooked in P. parsevalii) and large spatulate avicularia (subtriangular in P. parsevalii).Thus, here we reassign the Chinese specimens of P. parsevalii to P. pinctatae.Some records of P. egyptiaca made by Harmelin et al. [9,56] and Baradari et al. [18] also belong to P. pinctatae.The type specimen of P. egyptiaca (MFN Uncatalogued; Fig 11) is distinct from specimens characterized by these authors by having a raised secondary orifice, large avicularia with subtriangular profile and serrated margins and latero-oral avicularia oriented proximally.Thus, a review of specimens previously attributed to both P. parsevalii and P. egyptiaca and morphologically related is strongly recommended.

Parasmittina serrula
First described based on specimens from Hawaii, in the Central Pacific [2], P. serrula was already recorded from coral reefs of Belize, and experimental panels from Jamaica [3,37] in the Caribbean and several localities from the Western and Central Pacific [2].Although most reports of P. serrula from the Western and Central Pacific differ from the type specimens in characters of the primary orifice (Table 7), specimens from SW Atlantic studied here showed all morphological and morphometric characters provided by Soule & Soule [2] (Tables 6 and  7) to P. serrula.Its unusual geographical distribution was already related to hull shipping through the Panama Canal [16] and to an opportunistic behavior of the species [37].Among congeners, P. serrula is very similar to Parasmittina luteoserrula, recently described by Winston & Jackson [13] based on specimens from the Caribbean.Winston & Jackson [17] compared P. luteoserrula with P. serrula and indicated differences in the zooid sizes (indicated incorrectly as smaller in P. luteoserrula than in P. serrula, but zooids in the former species are actually larger, as shown in Table 6), large avicularia with a more fluted rostrum, and pores occupying more than half of the frontal surface of the ovicell.However, as previously discussed (see remarks of P. alba, for example), much of these variations may be related to different colonial and zooidal stages of development rather than different species.Thus, we consider a species complex involving P. serrula and P. luteoserrula, but additional studies including specimens from the current distributional range of P. serrula are needed.
Distribution.Central Pacific: Hawaii [3]; SW Atlantic: Brazil (present study).Remarks.Parasmittina simpulata was originally described based on a single infertile colony from southeastern Brazil, being diagnosed by having a primary orifice with distal denticles, serrated condyles, proximolateral small avicularia oval and subtriangular and large avicularia spatulate [12].All these characters are observed in specimens from coral reefs and experimental plates of tiles from northeastern Brazil analyzed in this study, adding that our Parasmittina simpulata is considered very similar to the Caribbean P. barbadensis Winston & Woollacott, 2009 [38], differing only in the large avicularia (absent in P. barbadensis) and larger zooids of P. barbadensis [12].Unfortunately, P. barbadensis was also described based on a single colony fragment, preventing more comparisons.Parasmittina simpulata and P. barbadensis also share similarities in the frontal calcification, primary and secondary orifices, and avicularia with P. parsevaliformis Soule & Soule, 1973 [2] described based on specimens from Hawaii, except for the large avicularium (absent in P. barbadensis) (Table 8).Soule & Soule [2] described differences in avicularia morphology and secondary calcification in the orifice and ovicell pending the colonial development of P. parsevaliformis.We also found morphological variations in the avicularia development and ovicell calcification when compared younger (Fig 13A and 13B) and older (Fig 13E and 13F) colonies.Also, our values comprise morphometric variations seen in the three taxa-P.simpulata, P. barbadensis and P. parsevaliformis (Table 8).Thus, we have some evidence that the absence of avicularia in specimens originally attributed to P. simpulata and P. barbadensis, respectively, as well as the morphometric variations, can be related to the ontogenetic stage of the studied specimens.

Parasmittina simpulata
Biogeographically, it is unlikely that P. simpulata (SW Atlantic), P. barbadensis (Caribbean), and P. parsevaliformis (Central Pacific) may represent a single species.On the other hand, P. parsevaliformis was described based on specimens that were encrusting a variety of substrata including rocks, corals, shells and cement [2] and material studied here include colonies from coral reefs and artificial substrata (experimental plates of tiles).Thus, the association with artificial substrata could suggest that a single species of Parasmittina may be dispersing worldwide, resulting in isolated geographical records.However, until more data on these taxa are known, we choose to keep them as distinct species.

Species
Like other species described here, P. winstonae haves an unusual geographic distribution in the Western and Central Pacific and SW Atlantic [8,12,45,57,58].Interestingly, Chinese and Brazilian specimens of P. winstonae showed a common association with bivalve shells of the genus Pinctada Ro ¨ding, 1798 [45,58].Colonies from Brazil studied here are also from artificial substrata, and specimens from Malaysia studied by Taylor & Tan [57] were encrusting shells on a rope hanging from a jetty.Therefore, passive dispersal may be related to the current distributional range of P. winstonae.
Diagnosis.Parasmittina with elliptical orifice, smooth distal margin, lyrula occupying three quarters of the orifice width, and robust downward-facing condyles with serrated margin.Secondary orifice low, forming side flaps without hiding the lyrula.Adventitious avicularia subtriangular smaller and large subspatulate to sublanceolate, with hooked tip, placed distolaterally to the orifice and with rostrum oriented proximolaterally.Ovicell globose with 20-32 medium-sized pseudopores distributed through the entire ovicell surface.
Other specimens of Parasmittina from Brazil were also attributed to Smittina trispinosa var.munita [23,33].Although these specimens have avicularia similar to that of P. falciformis sp.nov., differences among these taxa include the number of oral spines (3 in specimens from Marcus and 2 in P. falciformis sp.nov.), secondary orifice (shorter in P. falciformis sp.nov.), pseudosinus (shallower in P. falciformis), and rostrum of the small adventitious avicularia (straight in specimens from Marcus and curved in P. falciformis sp.nov.).Moreover, specimens studied by Marcus [23,34] have also a large interzooidal avicularia, not observed in P. falciformis sp.nov.Thus, here we consider that Smittina trispinosa var.munita described by Marcus [23,34] represent a distinct taxon than P. munita and P. facilformis sp.nov.
The combination of primary orifice with large lyrula, smooth distally, 1-2 oral spines, serrated condyles with hooked tips, and two types of avicularia distinguishes P. falciformis sp.nov.from all congeners.

Discussion
Although new species of Parasmittina from SW Atlantic have been described in the last years [10,11,12,13,59], we present the first review of historical records of the genus in the area.Additionally, to summarize the taxonomic knowledge regarding Parasmittina species worldwide, we compiled information on morphological features from the literature, mainly based on the original or subsequent descriptions of type specimens.This information is provided condyles profile and ornamentation, and lyrula and orifice width ratio), avicularia morphologies, ovicell size, and number of ovicell pores of 120 Parasmittina species (Table 10).Features of the primary orifice provided the most reliable taxonomic characters to distinguish Parasmittina species, as previously pointed out to the Indo-Pacific fauna by Tilbrook [8].The combination of distal margin and condyle ornamentations, number and profile of spines, and lyrula and orifice width ratio is unique to each species, including in the studied SW Atlantic taxa (Fig 16).Generally, most Parasmittina species have a smooth distal margin, 1-4 oral spines, robust and serrated condyles, and a lyrula occupying less than half of the orifice width.
Regarding avicularia, the small ones originated from latero-oral pores can be placed distoand/or proximolaterally to the orifice (Fig 17A -17D), and the small avicularia originated from marginal pores can be placed near zooidal margins and/or proximally in o the frontal wall (Fig 17E -17H).The large avicularium originated from a latero-oral pore and is typically placed proximolaterally to the orifice (Fig 18A -18H).
Avicularia of Parasmittina can be characterized in eight main types based on its morphologies: elongate (profile linear and narrow, with parallel margins, Fig 17A ); subtriangular (profile Most species of Parasmittina have one or two morphologies of small avicularia and only one morphology of large avicularia.However, several combinations of avicularia placements and morphologies are seen among taxa, with no apparent pattern correlating these features.For instance, based on the morphology of the small latero-oral avicularia, most Parasmittina species can be assigned in two groups-with oblong and/or subtriangular avicularia (as P. bimucronata, P. egyptiaca and P. simpulata) or with elongate avicularia (as P. abrolhosensis, P. areolata and P. spathulata).Only P. longirostrata and P. nasuta have small latero-oral avicularia oblong and/or elongate among all species.Also, the small elongate avicularia are always placed proximolaterally to the orifice, and most taxa with these avicularia lack a distolateral avicularium.
Interestingly, some nominal species can only be distinguished from congeners by characters that are known to differ pending on habitat and colonial development (i.e., [2,4,5,21]), mainly the number of oral spines or absence of avicularia-(P.alba, P. betamorphaea and P. lavela), (P.areolata and P. trunculata), (P.amazonensis, P. fraseri, P. indiginella and P. talismani), (P.barbadensis, P. parsevaliformis and P. simpulata), (P.longirostrata and P. serruloides), (P.serrula and P. luteoserrula).Thus, these little differences among taxa may represent intraspecific variations rather than different species.Currently, there are no integrative studies (combining morphology and moleculear analysis) to investigate species delimitation within the genus Parasmittina.Therefore, further studies including more colonies and other biological data, particularly molecular analysis, are needed to help clarify its taxonomic identity.Thus, to prevent to erect of new names and new synonymies based on characters that can be considered as intraspecific variations, here we choose to discuss and indicate the probable occurrence of species complex in Parasmittina, attributing the most appropriate available name to the studied SW Atlantic specimens and attempting to maintain some taxonomic stability in the genus.Analysis including colonies in different astogenetic stages, added with a precise characterization of the primary orifice, avicularia, and ovicells, are strongly required for a reliable taxonomic assignment (i.e., [2,4,5,9,17,21,38]).Among the eleven species of Parasmittina reported so far from the SW Atlantic, four species-P.betamorphaea, P. munita, P. spathulata and P. trispinosa-were not recognized in this study ( Fig 19).
Among species here recognized to occur in Brazil, five were originally described based on specimens from the area (P.abrolhosensis, P. alba, P. ligulata comb.nov., P. simpulata and P. falciformis sp.nov.).As mentioned previously, P. alba and P. simpulata are part of species complexes that need further investigation.The remaining species described here are mainly known from the Pacific.Due to the unexpected natural occurrence of P. bimucronata, P. longirostrata, P. pinctatae, P. serrula and P. winstonae in the SW Atlantic, we evaluated the exotic status of these species in the area (acc.[31]) (Table 11).One species was assigned as to be exotic (P.longirostrata), and the others were considered cryptogenic, including some (P.bimucronata, P. pinctatae and P. winstonae) previously misassigned to distinct species [10,11,12,26,53,58,60,61].These species are widespread along the Brazilian coast, growing on artificial and natural surfaces, indicating that these taxa are wellestablished in the studied area.Cryptogenic bryozoans must be treated as a cause of concern since, as exotic taxa, they can grow into dense colonies that can influence the associated and native fauna and have economic effects on human activities, including beaches usage, aquaculture, shipping, and fishing (acc.[15,31,62]).Thus, more studies with the species complexes recognized here are suggested to determine these taxa origin and help prevent bioinvasion events along the SW Atlantic., with the respective number of positive/negative criteria used.0, criterion not applicable due to lacking data; +, criterion applied positively to exotic status; −, criterion applied negatively to exotic status.N = number of attributes applied positively/negatively.Local criteria: 1 = local appearance where not found previously, 2 = local dispersal after introduction, 3 = association with human mechanisms of dispersal, 4 = prevalence or restriction to new or artificial environment, 5 = restricted distribution when compared to ecologically similar native species.Global criteria: 6 = widespread geographic distribution with isolated populations, 7 = active and passive dispersal mechanisms incapable of achieving the current distribution, 8 = exotic evolutionary origin.Status: E = exotic, C = cryptogenic.

Table 7 . Morphological variations in specimens from different localities assigned to P. serrula and P. luteoserrula.
Unknown states are assigned as (?).